Skip to main content
Log in

Volume-sensitive taurine transport in fish erythrocytes

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Taurine plays an important role in cell volume regulation in both vertebrates and invertebrates. Erythrocytes from two euryhaline fish species, the eel (Anguilla japonica) and the starry flounder (Platichthys stellatus) were found to contain high intracellular concentrations of this amino acid (≃ 30 mmol per liter of cell water). Kinetic studies established that the cells possessed a saturable high-affinity Na+-dependent β-amino-acid transport system which also required Cl for activity (apparentK m (taurine) 75 and 80 μm;V max 0.85 and 0.29 μmol/g Hb per hr for eel (20°C) and flounder cells (10°C), respectively. This β-system operated with an apparent Na+/Cl/taurine coupling ratio of 2∶1∶1. A reduction in extracellular osmolarity, leading to an increase in cell volume, reversibly decreased the activity of the transporter. In contrast, low medium osmolarity stimulated the activity of a Na+-independent nonsaturable transport route selective for taurine, γ-amino-n-butyric acid and small neutral amino acids, producing a net efflux of taurine from the cells. Neither component of taurine transport was detected in human erythrocytes. It is suggested that these functionally distinct transport routes participate in the osmotic regulation of intracellular taurine levels and hence contribute to the homeostatic regulation of cell volume. Volume-induced increases in Na+-independent taurine transport activity were suppressed by noradrenaline and 8-bromoadenosine-3′, 5′-cyclic monophosphate, but unaffected by the anticalmodulin drug, pimozide.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Baroin, A., Garcia-Romeu, F., Lamarre, T., Motais, R. 1984. Hormone-induced co-transport with specific pharmacological properties in erythrocytes of rainbow trout,Salmo gairdneri.J. Physiol. (London) 350:137–157

    Google Scholar 

  2. Baroin, A., Garcia-Romeu, F., Lamarre, T., Motais, R. 1984. A transient sodium-hydrogen exchange system induced by catecholamines in erythrocytes of rainbow trout,Salmo gairdneri.J. Physiol. (London) 356:21–31

    Google Scholar 

  3. Bourne, P.K., Cossins, A.R. 1982. On the instability of K+ influx in erythrocytes of the rainbow trout,Salmo gairdneri, and the role of catecholamine hormones in maintainingin vivo influx activity.J. Exp. Biol. 101:93–104

    PubMed  Google Scholar 

  4. Bourne, P.K., Cossins, A.R. 1984. Sodium and potassium transport in trout (Salmo gairdneri) erythrocytes.J. Physiol. (London) 347:361–375

    Google Scholar 

  5. Boyd, T.A., Cha, C.J., Forster, R.P., Goldstein, L. 1977. Free amino acids in tissues of the skateRaja erinacea and the stingrayDasyatis sabina: Effects of environmental dilution.J. Exp. Zool. 199:435–442

    PubMed  Google Scholar 

  6. Christensen, H.N. 1964. Relations in the transport of β-alanine and the α-amino acids in the Ehrlich cell.J. Biol. Chem. 239:3584–3589

    PubMed  Google Scholar 

  7. Christensen, H.N. 1969. Some special kinetic problems of transport.Adv. Enzymol. Relat. Areas Mol. Biol. 32:1–20

    PubMed  Google Scholar 

  8. Christensen, H.N. 1982. Interorgan amino acid nutrition.Phys. Rev. 62:1193–1233

    Google Scholar 

  9. Christensen, H.N. 1984. Organic ion transport during seven decades. The amino acids.Biochim. Biophys. Acta 779:225–269

    Google Scholar 

  10. Christensen, H.N., Antonioli, J.A. 1969. Cationic amino acid transport in the rabbit reticulocyte: Na+-dependent inhibition of Na+-independent transport.J. Biol. Chem. 244:1497–1504

    PubMed  Google Scholar 

  11. Cossins, A.R., Richardson, P.A. 1985. Adrenalin-induced Na+/H+ exchange in trout erythrocytes and its effects upon oxygen-carrying capacity.J. Exp. Biol. 118:229–246

    Google Scholar 

  12. DeVries, A.L., Ellory, J.C. 1982. The effect of stress on ion transport in fish erythrocytes.J. Physiol. (London) 324:51P

    Google Scholar 

  13. Dunham, P.B., Ellory, J.C. 1981. Passive potassium transport in low potassium sheep red cells: Dependence upon cell volume and chloride.J. Physiol. (London) 318:511–530

    Google Scholar 

  14. Eavenson, E., Christensen, H.N. 1967. Transport systems for neutral amino acids in the pigeon erythrocyte.J. Biol. Chem. 242:5386–5396

    PubMed  Google Scholar 

  15. Ellory, J.C., Jones, S.E.M., Preston, R.L., Young, J.D. 1981. A high-affinity sodium-dependent transport system for glutamate in dog red cells.J. Physiol. (London) 320:79P

    Google Scholar 

  16. Ellory, J.C., Jones, S.E.M., Young, J.D. 1983. Glycine transport in human erythrocytes.J. Physiol. (London) 320:403–422

    Google Scholar 

  17. Ellory, J.C., Preston, R.L., Young, J.D. 1983. Transport of amino acids for glutathione biosynthesis in human and dog red cells.Biomed. Biochim. Acta 42:S48-S52

    PubMed  Google Scholar 

  18. Ellory, J.C., Tucker, E.M., Deverson, E.V. 1972. The identification of ornithine and lysine at high concentrations in the red cells of sheep with an inherited deficiency of glutathione.Biochim. Biophys. Acta 279:481–483

    PubMed  Google Scholar 

  19. Fincham, D.A., Willis, J.S., Young, J.D. 1984. Red cell amino acid transport. Evidence for the presence of systemGly in guinea pig reticulocytes.Biochim. Biophys. Acta 777:147–150

    PubMed  Google Scholar 

  20. Fincham, D.A., Young, J.D., Mason, D.K., Collins, E.A., Snow, D.H. 1985. Breed and species comparison of amino acid transport variation in equine erythrocytes.Res. Vet. Sci. 38:346–351

    PubMed  Google Scholar 

  21. Forster, R.P., Goldstein, L. 1979. Amino acids and cell volume regulation.Yale J. Biol. Med. 52:497–515

    PubMed  Google Scholar 

  22. Fugelli, K. 1967. Regulation of cell volume in flounder (Pleuronectes flesus) erythrocytes accompanying a decrease in plasma osmolarity.Comp. Biochem. Physiol. 22:253–260

    PubMed  Google Scholar 

  23. Fugelli, K. 1970. Gamma-aminobutyric acid (GABA) in fish erythrocytes.Experientia 26:361

    Google Scholar 

  24. Fugelli, K., Riersen, L.O. 1978. Volume regulation in flounder erythrocytes. The effect of osmolality on taurine influx.In: Osmotic and Volume Regulation. Alfred Benzon Symposium XI. C.B. Jorgensen, and E. Skadhauge, editors. pp. 418–432. Munksgaard, Copenhagen

    Google Scholar 

  25. Fugelli, K., Rohrs, H. 1980. The effect of Na+ and osmolality on the influx and steady state distribution of taurine and gamma-aminobutyric acid in flounder (Platichthys flesus) erythrocytes.Comp. Biochem. Physiol. 67A:545–551

    Google Scholar 

  26. Fugelli, K., Zachariassen, K.E. 1976. The distribution of taurine, gamma-aminobutyric acid and inorganic ions between plasma and erythrocytes in flounder (Platichthys flesus) at different plasma osmolatities.Comp. Biochem. Physiol. 55A:173–177

    Google Scholar 

  27. Ginsburg, H., Krugliak, M. 1983. Uptake ofl-tryptophan by erythrocytes infected with malaria parasites (Plasmodium falciparum).Biochim. Biophys. Acta 729:97–103

    PubMed  Google Scholar 

  28. Gras, J., Gudefin, Y., Chagny, F., Perrier, H. 1982. Free amino acids and ninhydrin-positive substances in fish-II. Cardio-respiratory system: plasma, erythrocytes, heart and gills of the rainbow trout (Salmo gairdnerii Richardson).Comp. Biochem. Physiol. 73B:845–847

    Google Scholar 

  29. Hoffmann, E.K., Hendil, K.B. 1976. The role of amino acids and taurine in isosmotic intracellular regulation in Ehrlich ascites mouse tumor cells.J. Comp. Physiol. 108:279–286

    Google Scholar 

  30. Hoffmann, E.K., Lambert, I.H. 1983. Amino acid transport and cell volume regulation in Ehrlich ascites tumor cells.J. Physiol. (London) 338:613–625

    Google Scholar 

  31. Hoffmann, E.K., Simonsen, L.O., Lambert, I.H. 1984. Volume-induced increase of K+ and Cl permeabilities in Ehrlich ascites tumor cells. Role of internal Ca2+.J. Membrane Biol. 78:211–222

    Google Scholar 

  32. Imler, J.R., Vidaver, G.A. 1972. Anion effects on glycine entry into pigeon red blood cells.Biochim. Biophys. Acta 288:153–165

    PubMed  Google Scholar 

  33. Inaba, M., Maede, Y. 1984. Increase of Na+ gradient-dependentL-glutamate andL-aspartate transport in high K+ dog erythrocytes associated with high activity of (Na+, K+) ATPase.J. Biol. Chem. 259:312–317

    PubMed  Google Scholar 

  34. King, G.F., Kuchel, P.W. 1984. A proton NMR study of iminodipeptide transport and hydrolysis in the human erythrocyte: Possible physiological roles for the coupled system.Biochem. J. 220:553–560

    PubMed  Google Scholar 

  35. King, G.F., Kuchel, P.W. 1985. Assimilation of α-glutamylpeptides by human erythrocytes. A possible means of glutamate supply for glutathione synthesis.Biochem. J. 227:833–842

    PubMed  Google Scholar 

  36. King, G.F., York, M.J., Chapman, B.E., Kuchel, P.W. 1983. Proton NMR spectroscopic studies of dipeptidase in human erythrocytes.Biochem. Biophys. Res. Commun. 110:305–312

    PubMed  Google Scholar 

  37. Lambert, I.H. 1984. Na+-dependent taurine uptake in Ehrlich ascites tumor cells.Mol. Physiol. 6:233–246

    Google Scholar 

  38. Lambert, I.H. 1985. Taurine transport in Ehrlich ascites tumor cells. Specificity and chloride dependence.Mol. Physiol. 7:323–332

    Google Scholar 

  39. Maede, Y., Inaba, M., Taniguchi, N. 1983. Increase of Na-K-ATPase activity, glutamate and aspartate uptake in dog erythrocytes associated with hereditary high accumulation of GSH, glutamate, glutamine and aspartate.Blood 61:493–499

    PubMed  Google Scholar 

  40. Maede, Y., Kasai, N., Taniguchi, N. 1982. Hereditary high concentration of glutathione in canine erythrocytes associated with high accumulation of glutamate, glutamine and aspartate.Blood 59:883–889

    PubMed  Google Scholar 

  41. Palfrey, H.C., Rao, M.C. 1983. Na/K/Cl co-transport and its regulation.J. Exp. Biol. 106:43–54

    Google Scholar 

  42. Pierce, S.K. 1981. A symposium on cell volume regulation.J. Exp. Zool. 215:235–384

    PubMed  Google Scholar 

  43. Rudolph, S.A., Greengard, P. 1974. Regulation of protein phosphorylation and membrane permeability by β-adrenergic agents and cyclic adenosine 3′∶5′-monophosphate in the avian erythrocyte.J. Biol. Chem. 249:5684–5687

    PubMed  Google Scholar 

  44. Sherman, I.W. 1984. Metabolism.In: Anti-Malarial Drugs. I. Biological Background, Experimental Methods and Drug Resistence. W. Peters and W.H.G. Richards, editors. pp. 31–83. Springer, Berlin

    Google Scholar 

  45. Stein, W.D. 1986. Transport and Diffusion across Cell Membranes. pp. 231–361. Academic, New York

    Google Scholar 

  46. Tucker, E.M., Wright, P.C., Young, J.D. 1977. The influence of arginase deficiency on amino acid concentrations in sheep erythrocytes with a normal and a defective transport system for amino acids.J. Physiol. (London) 271:47P-48P

    Google Scholar 

  47. Tucker, E.M., Young, J.D. 1980. Biochemical changes during reticulocyte maturation in culture: A comparison of genetically different sheep erythrocytes.Biochem. J. 192:33–39

    PubMed  Google Scholar 

  48. Tucker, E.M., Young, J.D., Crowley, C. 1981. Red cell glutathione deficiency: Clinical and biochemical investigations using sheep as an experimental model system.Br. J. Haematol. 48:403–415

    PubMed  Google Scholar 

  49. Vidaver, G.A. 1964. Transport of glycine by pigeon red blood cells.Biochemistry 3:662–667

    Google Scholar 

  50. Vidaver, G.A., Shepherd, S.L., Lagow, J.B., Weichelman, K.J. 1976. Glycine transport by haemolysed and restored pigeon red cells. Effects of a Donnan-induced electrical potential on entry and exit kinetics.Biochim. Biophys. Acta 443:494–514

    PubMed  Google Scholar 

  51. Vislie, T. 1980. Cell volume regulation in isolated, perfused heart ventricle of the flounder (Platichthys flesus), Comp. Biochem. Physiol. 65A:19–27

    Google Scholar 

  52. Vislie, T., Fugelli, K. 1975. Cell volume regulation in flounder (Platichthys flesus) heart muscle accompanying an alteration in plasma osmolality.Comp. Biochem. Physiol. 52A:415–418

    Google Scholar 

  53. Weiss, B., Prozialeck, W., Cimino, M., Barnette, M.S., Wallace, T.L. 1980. Pharmacological regulation of calmodulin.In: Calmodulin and Cell Functions. D.M. Watterson and F.F. Vincenzi, editors.Ann. N.Y. Acad. Sci. 356:319–345

  54. Wheeler, K.P., Christensen, H.N. 1967. Interdependent fluxes of amino acids and sodium ion in the pigeon red blood cell.J. Biol. Chem. 242:3782–3788

    PubMed  Google Scholar 

  55. Winter, C.G., Christensen, H.N. 1965. Contrasts in neutral amino acid transport by rabbit erythrocytes and reticulocytes.J. Biol. Chem. 240:3594–3600

    PubMed  Google Scholar 

  56. Young, J.D. 1983. Erythrocyte amino acid and nucleoside transport.In: Red Blood Cells of Domestic Animals. N.S. Agar and P.G. Board, editors. pp. 271–290. Elsevier Science, Amsterdam

    Google Scholar 

  57. Young, J.D., Ellory, J.C. 1977. Substrate specificity of amino acid transport in sheep erythrocytes.Biochem. J. 162:33–38

    PubMed  Google Scholar 

  58. Young, J.D., Ellory, J.C. 1977. Red cell amino acid transport.In: Membrane Transport in Red Cells. J.C. Ellory and V.L. Lew, editors. pp. 301–325. Academic, London

    Google Scholar 

  59. Young, J.D., Ellory, J.C. 1982. Flux measurements.In: Red Cell Membranes. A Methodological Approach. J.C. Ellory and J.d. Young, editors. pp. 119–133. Academic, London

    Google Scholar 

  60. Young, J.D., Tucker, E.M. 1983. Erythrocyte glutathione deficiency in sheep.In: Functions of Glutathione: Biochemical, Physiological, Toxicological and Clinical Aspects. A. Larsson, S. Orrenius, A. Holmgren, and B. Mannervik, editors. pp. 373–384. Raven, New York

    Google Scholar 

  61. Young, J.D., Tucker, E.M., Kilgour, L. 1982. Genetic control of amino acid transport in sheep erythrocytes.Biochem. Genet. 20:723–731

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fincham, D.A., Wolowyk, M.W. & Young, J.D. Volume-sensitive taurine transport in fish erythrocytes. J. Membrain Biol. 96, 45–56 (1987). https://doi.org/10.1007/BF01869333

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01869333

Key Words

Navigation